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received: 22 May 2015 accepted: 10 December 2015 Published: 20 January 2016
Why I tense up when you watch me: Inferior parietal cortex mediates an audience’s influence on motor performance Michiko Yoshie1,2,3,4,5, Yoko Nagai3, Hugo D. Critchley3,6 & Neil A. Harrison3,6 The presence of an evaluative audience can alter skilled motor performance through changes in force output. To investigate how this is mediated within the brain, we emulated real-time social monitoring of participants’ performance of a fine grip task during functional magnetic resonance neuroimaging. We observed an increase in force output during social evaluation that was accompanied by focal reductions in activity within bilateral inferior parietal cortex. Moreover, deactivation of the left inferior parietal cortex predicted both inter- and intra-individual differences in socially-induced change in grip force. Social evaluation also enhanced activation within the posterior superior temporal sulcus, which conveys visual information about others’ actions to the inferior parietal cortex. Interestingly, functional connectivity between these two regions was attenuated by social evaluation. Our data suggest that social evaluation can vary force output through the altered engagement of inferior parietal cortex; a region implicated in sensorimotor integration necessary for object manipulation, and a component of the action-observation network which integrates and facilitates performance of observed actions. Social-evaluative situations may induce high-level representational incoherence between one’s own intentioned action and the perceived intention of others which, by uncoupling the dynamics of sensorimotor facilitation, could ultimately perturbe motor output. The visible anguish of an athlete whose performance falters at a critical moment conveys the powerful effects that an evaluative audience can exert on motor performance. Empirical evidence suggests that effects of an audience on behaviour can be either facilitative or detrimental, depending on a variety of factors including task demands, performance context, and personality traits1–4. With regard to the type of motor skills, the presence of an audience tends to improve performance of simple (well-learned) tasks such as running and weightlifting1,5,6. However, this socially-induced enhancement of motor output can impair performance of more complex tasks requiring coordination abilities5,7,8. For instance, previous studies8,9 have shown that the performance quality of skilled pianists deteriorates both technically and artistically, when playing in front of an evaluative audience compared to when playing alone. Further, measurements of electromyographic activity have indicated that persistent low-level muscle tension in the arm and shoulder, induced by the presence of an audience, can lead to increased keystroke force resulting in a loss of fine control of dynamics and temporal fluency within musical performances8–10. Although such social effects on motor control are well-documented, the central neural mechanisms through which the presence of observers increases force output have not previously been studied. To address this, we devised a simple motor task, which was an adaption of earlier pinch- and power-grip tasks11–14 and was designed to capture subtle changes in tonic muscle tension evoked by the presence of an evaluative audience (Fig. 1). We presented two levels of task demand: we asked participants to produce two different levels of grip force, namely 5% or 10% of maximal voluntary contraction (MVC). 1
Human Informatics Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, 305-8566, Japan. 2Automotive Human Factors Research Center, AIST, Tsukuba, 305-8566, Japan. 3 Department of Psychiatry, Brighton and Sussex Medical School, Brighton, BN1 9RR, United Kingdom. 4Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, 153-8902, Japan. 5Graduate School of Frontier Biosciences, Osaka University, Osaka, 565-0871, Japan. 6Sackler Centre for Consciousness Science, University of Sussex, Brighton, United Kingdom. Correspondence and requests for materials should be addressed to M.Y. (email:
[email protected]) Scientific Reports | 6:19305 | DOI: 10.1038/srep19305
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Figure 1. Experimental task. Participants first viewed a thermometer and adjusted their grip force (blue liquid) to match the target force (5% or 10% of their maximal voluntary contraction or MVC, red line) for 5 s. They then tried to maintain the target force for 15 s while viewing a video of two judges apparently monitoring either their own (observed condition) or another participant’s performance (unobserved condition). The lower panel shows a typical example of participants’ performance during the 10% MVC task. Progressive force decay was quantified by subtracting target from actual force (force error). Participants produced stronger grip force in the observed (red) compared to unobserved (blue) condition.
The presence or absence of social evaluation was experimentally manipulated by presenting each participant with video footage of two observers who appeared to be closely evaluating the participant’s own task performance in real-time (observed condition) or that of another participant (unobserved condition). We predicted that the observed condition would elicit a mild level of anxiety in our participants, as in previous studies8,9. All conditions were implemented within a human functional magnetic resonance imaging (fMRI) environment. By minimising the difference in visual properties of the stimuli used in the two social conditions, we aimed to quantify changes in regional brain activity reflecting effects of social evaluation. When the presence of evaluative observers influences our motor behaviour, visual information relating to the feelings and intentions of these individuals (e.g., facial expressions, direction of gaze) first needs to be processed in the brain. Previous studies both in monkeys and humans have identified the posterior superior temporal sulcus (pSTS) as a key neural substrate for social perception based on visual cues15–17. The pSTS region is known to be activated by actual or implied biological motion (e.g., movements of the eyes, mouth, hands, and body) and also by facial expressions15,18. Since social evaluation would likely facilitate the processing of these social cues, we predicted that the observed condition would elicit increased activation within the pSTS region. The inferior parietal cortex (IPC) forms part of the frontoparietal network, and via its anatomical connections with the ventral premotor cortex (PMv) is involved in the sensorimotor transformations necessary for object grasping and manipulation19. Given our use of a similar isometric grip task, we hypothesised that effects of social evaluation on motor performance would be mediated via actions on the IPC. Supporting this prediction, during social observation processing of social features within the pSTS region is known to be conveyed to the IPC, which is then capable of generating appropriate motor actions based on the social cues20. We thus investigated whether activity within the IPC is modulated in relation to the inter- and intra-individual variability in the effects of social evaluation on force output.
Scientific Reports | 6:19305 | DOI: 10.1038/srep19305
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Figure 2. Behavioural results. (a) Mean self-rated anxiety score showing a significant increase in anxiety in the observed condition. (b) Mean force error. Force error data for each 1-s period of social video presentation were averaged across trials and participants for each condition. During the 10% MVC task isometric grip force was significantly increased in the observed (red solid line) compared to unobserved condition (blue solid line). However, during the 5% MVC task force level did not significantly differ between the observed (red dashed line) and unobserved (blue dashed line) conditions at the group level. Data are represented as mean ± SEM. ***p
